Home LiteratureArticle Details
PMID: 18398507 Published · ppublish English Journal Article

Antibody association with HER-2/neu-targeted vaccine enhances CD8 T cell responses in mice through Fc-mediated activation of DCs.

The Journal of clinical investigation ·Vol. 118 ·No. 5 ·2008-05-00 ·Pages 1700-11

Kim PS, Armstrong TD, Song H, Wolpoe ME, Weiss V, Manning EA, Huang LQ, Murata S, Sgouros G, Emens LA, Reilly RT, Jaffee EM

Abstract

The pathogenic nature of cancer is attributed, at least in part, to the ability of tumors cells to induce systemic and local mechanisms of immune tolerance. However, we previously reported that tumor-free survival in up to 100% of tolerized HER-2/neu transgenic mice can be achieved by administration of neu-specific mAb concurrently with a HER-2/neu-expressing, GM-CSF-secreting whole cell vaccine. In this report, we show that one mechanism of improved antitumor activity induced by the combination of these 2 neu-targeted interventions was enhanced Fc-mediated activation of APCs. Specifically, in vivo studies demonstrated localization of radiolabeled neu-specific mAb at the vaccine site. Subsequently, increased accumulation of neu-specific mAb at the vaccine-draining lymph node correlated with increased vaccine cell uptake by DCs in vivo. This led to enhancement of CD8(+) neu-specific T cell function in terms of proliferation, cytokine production, and central memory development. Thus, the administration of a neu-specific mAb with a neu-targeted GM-CSF-secreting tumor vaccine enhanced induction of neu-specific CD8(+) T cells through Fc-mediated activation of DCs. This multimodality attack on the same tumor antigen may have the potential to overcome tolerance to self antigens and weaken the immunosuppressive networks within the tumor microenvironment.

MeSH Terms
Adoptive Transfer Animals Antibodies, Monoclonal/immunology,therapeutic use CD11c Antigen/immunology CD8-Positive T-Lymphocytes/cytology,immunology Cancer Vaccines/immunology Cell Line Dendritic Cells/cytology,immunology Female Granulocyte-Macrophage Colony-Stimulating Factor/metabolism Immunoglobulin Fc Fragments/immunology Mice Mice, Transgenic Neoplasms/immunology,pathology Receptor, ErbB-2/genetics,immunology Survival Rate
Chemicals
Antibodies, Monoclonal CD11c Antigen Cancer Vaccines Immunoglobulin Fc Fragments Granulocyte-Macrophage Colony-Stimulating Factor Receptor, ErbB-2
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Kim Peter S
The Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, 1650 Orleans Street, CRB1 4M86, Baltimore, Maryland 21231, USA. pskim07@gmail.com
Armstrong Todd D
Song Hong
Wolpoe Matthew E
Weiss Vivian
Manning Elizabeth A
Huang Lan Qing
Murata Satoshi
Sgouros George
Emens Leisha A
Reilly R Todd
Jaffee Elizabeth M
References (48)
48 references, click to expand
  1. Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease.
    Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):10578-82 PMID: 1359541
  2. Leveraging the activity of tumor vaccines with cytotoxic chemotherapy.
    Cancer Res. 2005 Sep 15;65(18):8059-64 PMID: 16166275
  3. Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcgammaRIIIa gene.
    Blood. 2002 Feb 1;99(3):754-8 PMID: 11806974
  4. Antitumor monoclonal antibodies enhance cross-presentation ofcCellular antigens and the generation of myeloma-specific killer T cells by dendritic cells.
    J Exp Med. 2002 Jan 7;195(1):125-33 PMID: 11781371
  5. Selective blockade of inhibitory Fcgamma receptor enables human dendritic cell maturation with IL-12p70 production and immunity to antibody-coated tumor cells.
    Proc Natl Acad Sci U S A. 2005 Feb 22;102(8):2910-5 PMID: 15703291
  6. Naturally-occurring CD4+CD25+ immunoregulatory T cells: central players in the arena of peripheral tolerance.
    Semin Immunol. 2004 Apr;16(2):81-8 PMID: 15036231
  7. Neoadjuvant trastuzumab induces apoptosis in primary breast cancers.
    J Clin Oncol. 2005 Apr 10;23(11):2460-8 PMID: 15710948
  8. Accelerated antigen presentation and elicitation of humoral response in vivo by FcgammaRIIB- and FcgammaRI/III-mediated immune complex uptake.
    Cell Immunol. 2003 Sep;225(1):21-32 PMID: 14643301
  9. Antigen-specific inhibition of CD8+ T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species.
    J Immunol. 2004 Jan 15;172(2):989-99 PMID: 14707072
  10. Regulatory T cells and cancer.
    Curr Opin Immunol. 2007 Apr;19(2):217-23 PMID: 17306521
  11. Inducing tumor immunity through the selective engagement of activating Fcgamma receptors on dendritic cells.
    J Exp Med. 2002 Jun 17;195(12):1653-9 PMID: 12070293
  12. Mechanisms of immune evasion by tumors.
    Adv Immunol. 2006;90:51-81 PMID: 16730261
  13. Antigen-antibody immune complexes empower dendritic cells to efficiently prime specific CD8+ CTL responses in vivo.
    J Immunol. 2002 Mar 1;168(5):2240-6 PMID: 11859111
  14. Immune resistance orchestrated by the tumor microenvironment.
    Immunol Rev. 2006 Oct;213:131-45 PMID: 16972901
  15. CD20 antibody (C2B8)-induced apoptosis of lymphoma cells promotes phagocytosis by dendritic cells and cross-priming of CD8+ cytotoxic T cells.
    Leukemia. 2001 Oct;15(10):1619-26 PMID: 11587221
  16. Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets.
    Nat Med. 2000 Apr;6(4):443-6 PMID: 10742152
  17. Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colony-stimulating factor stimulates potent, specific, and long-lasting anti-tumor immunity.
    Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3539-43 PMID: 8097319
  18. Fcgamma receptor-mediated induction of dendritic cell maturation and major histocompatibility complex class I-restricted antigen presentation after immune complex internalization.
    J Exp Med. 1999 Jan 18;189(2):371-80 PMID: 9892619
  19. Monoclonal antibody therapy.
    Front Biosci. 2006 May 01;11:1620-35 PMID: 16368542
  20. Identification and characterization of the immunodominant rat HER-2/neu MHC class I epitope presented by spontaneous mammary tumors from HER-2/neu-transgenic mice.
    J Immunol. 2003 Apr 15;170(8):4273-80 PMID: 12682262
  21. Trastuzumab-mediated antibody-dependent cellular cytotoxicity against esophageal squamous cell carcinoma.
    Clin Cancer Res. 2005 Jul 1;11(13):4898-904 PMID: 16000588
  22. A rapid, single vessel method for preparation of clinical grade ligand conjugated monoclonal antibodies.
    Nucl Med Biol. 1995 Apr;22(3):387-90 PMID: 7627155
  23. Role of immature myeloid cells in mechanisms of immune evasion in cancer.
    Cancer Immunol Immunother. 2006 Mar;55(3):237-45 PMID: 16047143
  24. Differential antigen processing by dendritic cell subsets in vivo.
    Science. 2007 Jan 5;315(5808):107-11 PMID: 17204652
  25. Two immunoglobulin G fragment C receptor polymorphisms independently predict response to rituximab in patients with follicular lymphoma.
    J Clin Oncol. 2003 Nov 1;21(21):3940-7 PMID: 12975461
  26. Immune complex-mediated antigen presentation induces tumor immunity.
    J Clin Invest. 2002 Jul;110(1):71-9 PMID: 12093890
  27. The exploitation of distinct recognition receptors in dendritic cells determines the full range of host immune relationships with Candida albicans.
    Int Immunol. 2004 Jan;16(1):149-61 PMID: 14688070
  28. Genes to vaccines for immunotherapy: how the molecular biology revolution has influenced cancer immunology.
    Mol Cancer Ther. 2005 Nov;4(11):1645-52 PMID: 16275985
  29. Cyclophosphamide, doxorubicin, and paclitaxel enhance the antitumor immune response of granulocyte/macrophage-colony stimulating factor-secreting whole-cell vaccines in HER-2/neu tolerized mice.
    Cancer Res. 2001 May 1;61(9):3689-97 PMID: 11325840
  30. Generation, migration and function of circulating dendritic cells.
    Curr Opin Immunol. 2006 Aug;18(4):503-11 PMID: 16777395
  31. The collaboration of both humoral and cellular HER-2/neu-targeted immune responses is required for the complete eradication of HER-2/neu-expressing tumors.
    Cancer Res. 2001 Feb 1;61(3):880-3 PMID: 11221874
  32. Constitutive versus activation-dependent cross-presentation of immune complexes by CD8(+) and CD8(-) dendritic cells in vivo.
    J Exp Med. 2002 Sep 16;196(6):817-27 PMID: 12235214
  33. A vascular endothelial growth factor receptor-2 inhibitor enhances antitumor immunity through an immune-based mechanism.
    Clin Cancer Res. 2007 Jul 1;13(13):3951-9 PMID: 17606729
  34. Transcutaneous immunization induces mucosal CTLs and protective immunity by migration of primed skin dendritic cells.
    J Clin Invest. 2004 Apr;113(7):998-1007 PMID: 15057306
  35. Immune complex-loaded dendritic cells are superior to soluble immune complexes as antitumor vaccine.
    J Immunol. 2006 Apr 15;176(8):4573-80 PMID: 16585547
  36. CD4 and CD8 expression by human and mouse thymic dendritic cells.
    Immunol Lett. 1994 May;40(2):93-9 PMID: 8088877
  37. Distinct pathways of antigen uptake and intracellular routing in CD4 and CD8 T cell activation.
    Science. 2007 Apr 27;316(5824):612-6 PMID: 17463291
  38. Central tolerance: good but imperfect.
    Immunol Rev. 2006 Feb;209:290-6 PMID: 16448550
  39. Physiologic regulation of central and peripheral T cell tolerance: lessons for therapeutic applications.
    J Mol Med (Berl). 2006 Nov;84(11):887-99 PMID: 16972086
  40. The induction of systemic and mucosal immune responses to antigen-adjuvant compositions administered into the skin: alterations in the migratory properties of dendritic cells appears to be important for stimulating mucosal immunity.
    Vaccine. 2000 Jun 1;18(24):2753-67 PMID: 10781863
  41. Smoldering and polarized inflammation in the initiation and promotion of malignant disease.
    Cancer Cell. 2005 Mar;7(3):211-7 PMID: 15766659
  42. Class I-restricted presentation of exogenous antigen acquired by Fcgamma receptor-mediated endocytosis is regulated in dendritic cells.
    Eur J Immunol. 2000 Mar;30(3):848-57 PMID: 10741401
  43. HER-2/neu-specific monoclonal antibodies collaborate with HER-2/neu-targeted granulocyte macrophage colony-stimulating factor secreting whole cell vaccination to augment CD8+ T cell effector function and tumor-free survival in Her-2/neu-transgenic mice.
    J Immunol. 2003 Aug 15;171(4):2161-9 PMID: 12902523
  44. Phagocytosis requires repeated triggering of macrophage phagocytic receptors during particle ingestion.
    Nature. 1981 Jan 29;289(5796):409-11 PMID: 7464909
  45. HER-2/neu is a tumor rejection target in tolerized HER-2/neu transgenic mice.
    Cancer Res. 2000 Jul 1;60(13):3569-76 PMID: 10910070
  46. Central memory and effector memory T cell subsets: function, generation, and maintenance.
    Annu Rev Immunol. 2004;22:745-63 PMID: 15032595
  47. Cancer cell immune escape and tumor progression by exploitation of anti-inflammatory and pro-inflammatory responses.
    Cancer Biol Ther. 2005 Sep;4(9):924-33 PMID: 16177562
  48. Targeting apoptotic tumor cells to Fc gamma R provides efficient and versatile vaccination against tumors by dendritic cells.
    J Immunol. 2003 Feb 15;170(4):1641-8 PMID: 12574326
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
2008-05-00
Pages
1700-11
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC2289797
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com